Engineering approaches to illuminating brain structure and dynamics

Neuron

Volumn 80, Issue 3, 2013, Pages 568-577

  Deisseroth, Karl ^a,b   Schnitzer, Mark J ^b  

^a Stanford University   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GREEN FLUORESCENT PROTEIN;

BIOENGINEERING; BRAIN FUNCTION; BRAIN TISSUE; ENDOPLASMIC RETICULUM; MOUSE; NERVOUS SYSTEM; NEUROSCIENCE; NONHUMAN; PRIORITY JOURNAL; PROTEIN ENGINEERING; PROTEIN TARGETING; REVIEW; SIGNAL DETECTION;

ANIMALS; BIOENGINEERING; BRAIN; HISTORY, 20TH CENTURY; HISTORY, 21ST CENTURY; HUMANS; NEUROSCIENCES; NONLINEAR DYNAMICS;

EID: 84887002027     PISSN: 08966273     EISSN: 10974199     Source Type: Journal    
DOI: 10.1016/j.neuron.2013.10.032     Document Type: Review

References (93)

1. Ahrens M.B., Orger M.B., Robson D.N., Li J.M., Keller P.J. Whole-brain functional imaging at cellular resolution using light-sheet microscopy. Nat. Methods 2013, 10:413-420.
2. Akerboom J., Carreras Calderón N., Tian L., Wabnig S., Prigge M., Tolö J., Gordus A., Orger M.B., Severi K.E., Macklin J.J., et al. Genetically encoded calcium indicators for multi-color neural activity imaging and combination with optogenetics. Front Mol Neurosci 2013, 6:2.
3. Albrecht D.R., Bargmann C.I. High-content behavioral analysis of Caenorhabditis elegans in precise spatiotemporal chemical environments. Nat. Methods 2011, 8:599-605.
4. Alivisatos A.P., Andrews A.M., Boyden E.S., Chun M., Church G.M., Deisseroth K., Donoghue J.P., Fraser S.E., Lippincott-Schwartz J., Looger L.L., et al. Nanotools for neuroscience and brain activity mapping. ACS Nano 2013, 7:1850-1866.
5. Anikeeva P., Andalman A.S., Witten I., Warden M., Goshen I., Grosenick L., Gunaydin L.A., Frank L.M., Deisseroth K. Optetrode: a multichannel readout for optogenetic control in freely moving mice. Nat. Neurosci. 2012, 15:163-170.
6. Bamann C., Gueta R., Kleinlogel S., Nagel G., Bamberg E. Structural guidance of the photocycle of channelrhodopsin-2 by an interhelical hydrogen bond. Biochemistry 2010, 49:267-278.
7. Bepari A.K., Sano H., Tamamaki N., Nambu A., Tanaka K.F., Takebayashi H. Identification of optogenetically activated striatal medium spiny neurons by Npas4 expression. PLoS ONE 2012, 7:e52783.
8. Berndt A., Yizhar O., Gunaydin L.A., Hegemann P., Deisseroth K. Bi-stable neural state switches. Nat. Neurosci. 2009, 12:229-234.
9. Berndt A., Schoenenberger P., Mattis J., Tye K.M., Deisseroth K., Hegemann P., Oertner T.G. High-efficiency channelrhodopsins for fast neuronal stimulation at low light levels. Proc. Natl. Acad. Sci. USA 2011, 108:7595-7600.
10. Bertolotti J., van Putten E.G., Blum C., Lagendijk A., Vos W.L., Mosk A.P. Non-invasive imaging through opaque scattering layers. Nature 2012, 491:232-234.
11. Broxton M., Grosenick L., Yang S., Cohen N., Andalman A., Deisseroth K., Levoy M. Wave optics theory and 3-D deconvolution for the light field microscope. Opt. Express 2013, 21:25418-25439.
12. Cao G., Platisa J., Pieribone V.A., Raccuglia D., Kunst M., Nitabach M.N. Genetically targeted optical electrophysiology in intact neural circuits. Cell 2013, 154:904-913.
13. Carter M.E., Brill J., Bonnavion P., Huguenard J.R., Huerta R., de Lecea L. Mechanism for Hypocretin-mediated sleep-to-wake transitions. Proc. Natl. Acad. Sci. USA 2012, 109:E2635-E2644.
14. Cha C., Liechty W.B., Khademhosseini A., Peppas N.A. Designing biomaterials to direct stem cell fate. ACS Nano 2012, 6:9353-9358.
15. Chan D.P., Deleavey G.F., Owen S.C., Damha M.J., Shoichet M.S. Click conjugated polymeric immuno-nanoparticles for targeted siRNA and antisense oligonucleotide delivery. Biomaterials 2013, 34:8408-8415.
16. Chang T.Y., Pardo-Martin C., Allalou A., Wählby C., Yanik M.F. Fully automated cellular-resolution vertebrate screening platform with parallel animal processing. Lab Chip 2012, 12:711-716.
17. Chung K., Deisseroth K. CLARITY for mapping the nervous system. Nat. Methods 2013, 10:508-513.
18. Chung K., Kim Y., Kanodia J.S., Gong E., Shvartsman S.Y., Lu H. A microfluidic array for large-scale ordering and orientation of embryos. Nat. Methods 2011, 8:171-176.
19. Chung K., Zhan M., Srinivasan J., Sternberg P.W., Gong E., Schroeder F.C., Lu H. Microfluidic chamber arrays for whole-organism behavior-based chemical screening. Lab Chip 2011, 11:3689-3697.
20. Chung K., Wallace J., Kim S.Y., Kalyanasundaram S., Andalman A.S., Davidson T.J., Mirzabekov J.J., Zalocusky K.A., Mattis J., Denisin A.K., et al. Structural and molecular interrogation of intact biological systems. Nature 2013, 497:332-337.
21. Dangi S., Orsborn A.L., Moorman H.G., Carmena J.M. Design and analysis of closed-loop decoder adaptation algorithms for brain-machine interfaces. Neural Comput. 2013, 25:1693-1731.
22. Dani A., Huang B., Bergan J., Dulac C., Zhuang X. Superresolution imaging of chemical synapses in the brain. Neuron 2010, 68:843-856.
23. Deisseroth K. Optogenetics. Nat. Methods 2011, 8:26-29.
24. Dufour S., Lavertu G., Dufour-Beauséjour S., Juneau-Fecteau A., Calakos N., Deschênes M., Vallée R., De Koninck Y. A multimodal micro-optrode combining field and single unit recording, multispectral detection and photolabeling capabilities. PLoS ONE 2013, 8:e57703.
25. Farrar M.J., Wise F.W., Fetcho J.R., Schaffer C.B. Invivo imaging of myelin in the vertebrate central nervous system using third harmonic generation microscopy. Biophys. J. 2011, 100:1362-1371.
26. Fenno L., Yizhar O., Deisseroth K. The development and application of optogenetics. Annu. Rev. Neurosci. 2011, 34:389-412.
27. Ferreira L.S., Gerecht S., Fuller J., Shieh H.F., Vunjak-Novakovic G., Langer R. Bioactive hydrogel scaffolds for controllable vascular differentiation of human embryonic stem cells. Biomaterials 2007, 28:2706-2717.
28. Ghosh K.K., Burns L.D., Cocker E.D., Nimmerjahn A., Ziv Y., Gamal A.E., Schnitzer M.J. Miniaturized integration of a fluorescence microscope. Nat. Methods 2011, 8:871-878.
29. Gilja V., Chestek C.A., Diester I., Henderson J.M., Deisseroth K., Shenoy K.V. Challenges and opportunities for next-generation intracortically based neural prostheses. IEEE Trans. Biomed. Eng. 2011, 58:1891-1899.
30. Godara P., Dubis A.M., Roorda A., Duncan J.L., Carroll J. Adaptive optics retinal imaging: emerging clinical applications. Optom. Vis. Sci. 2010, 87:930-941.
31. Gong Y., Li J.Z., Schnitzer M.J. Enhanced Archaerhodopsin Fluorescent Protein Voltage Indicators. PLoS ONE 2013, 8:e66959.
32. Gradinaru V., Thompson K.R., Zhang F., Mogri M., Kay K., Schneider M.B., Deisseroth K. Targeting and readout strategies for fast optical neural control invitro and invivo. J.Neurosci. 2007, 27:14231-14238.
33. Gradinaru V., Thompson K.R., Deisseroth K. eNpHR: a Natronomonas halorhodopsin enhanced for optogenetic applications. Brain Cell Biol. 2008, 36:129-139.
34. Gradinaru V., Zhang F., Ramakrishnan C., Mattis J., Prakash R., Diester I., Goshen I., Thompson K.R., Deisseroth K. Molecular and cellular approaches for diversifying and extending optogenetics. Cell 2010, 141:154-165.
35. Gunaydin L.A., Yizhar O., Berndt A., Sohal V.S., Deisseroth K., Hegemann P. Ultrafast optogenetic control. Nat. Neurosci. 2010, 13:387-392.
36. Haikala V., Joesch M., Borst A., Mauss A.S. Optogenetic control of fly optomotor responses. J.Neurosci. 2013, 33:13927-13934.
37. Hall L.T., Beart G.C., Thomas E.A., Simpson D.A., McGuinness L.P., Cole J.H., Manton J.H., Scholten R.E., Jelezko F., Wrachtrup J., et al. High spatial and temporal resolution wide-field imaging of neuron activity using quantum NV-diamond. Sci Rep 2012, 2:401.
38. Heim R., Cubitt A.B., Tsien R.Y. Improved green fluorescence. Nature 1995, 373:663-664.
39. Hochberg L.R., Bacher D., Jarosiewicz B., Masse N.Y., Simeral J.D., Vogel J., Haddadin S., Liu J., Cash S.S., van der Smagt P., Donoghue J.P. Reach and grasp by people with tetraplegia using a neurally controlled robotic arm. Nature 2012, 485:372-375.
40. Horton N.G., Wang K., Kobat D., Clark C.G., Wise F.W., Schaffer C.B., Xu C. Invivo three-photon microscopy of subcortical structures within an intact mouse brain. Nat. Photonics 2013, 7:205-209.
41. Hunter J.J., Masella B., Dubra A., Sharma R., Yin L., Merigan W.H., Palczewska G., Palczewski K., Williams D.R. Images of photoreceptors in living primate eyes using adaptive optics two-photon ophthalmoscopy. Biomed. Opt. Express 2010, 2:139-148.
42. Jeong D.C., Tsai P.S., Kleinfeld D. Prospect for feedback guided surgery with ultra-short pulsed laser light. Curr. Opin. Neurobiol. 2012, 22:24-33.
43. Ji N., Sato T.R., Betzig E. Characterization and adaptive optical correction of aberrations during invivo imaging in the mouse cortex. Proc. Natl. Acad. Sci. USA 2012, 109:22-27.
44. Jin L., Han Z., Platisa J., Wooltorton J.R., Cohen L.B., Pieribone V.A. Single action potentials and subthreshold electrical events imaged in neurons with a fluorescent protein voltage probe. Neuron 2012, 75:779-785.
45. Kabra M., Robie A.A., Rivera-Alba M., Branson S., Branson K. JAABA: interactive machine learning for automatic annotation of animal behavior. Nat. Methods 2013, 10:64-67.
46. Kato H.E., Zhang F., Yizhar O., Ramakrishnan C., Nishizawa T., Hirata K., Ito J., Aita Y., Tsukazaki T., Hayashi S., et al. Crystal structure of the channelrhodopsin light-gated cation channel. Nature 2012, 482:369-374.
47. Keplinger C., Sun J.Y., Foo C.C., Rothemund P., Whitesides G.M., Suo Z. Stretchable, transparent, ionic conductors. Science 2013, 341:984-987.
48. Kim D.H., Ghaffari R., Lu N., Rogers J.A. Flexible and stretchable electronics for biointegrated devices. Annu. Rev. Biomed. Eng. 2012, 14:113-128.
49. Kim T.I., McCall J.G., Jung Y.H., Huang X., Siuda E.R., Li Y., Song J., Song Y.M., Pao H.A., Kim R.H., et al. Injectable, cellular-scale optoelectronics with applications for wireless optogenetics. Science 2013, 340:211-216.
50. Kobat D., Durst M.E., Nishimura N., Wong A.W., Schaffer C.B., Xu C. Deep tissue multiphoton microscopy using longer wavelength excitation. Opt. Express 2009, 17:13354-13364.
51. Kobat D., Horton N.G., Xu C. Invivo two-photon microscopy to 1.6-mm depth in mouse cortex. J.Biomed. Opt. 2011, 16:106014.
52. Konermann S., Brigham M.D., Trevino A.E., Hsu P.D., Heidenreich M., Cong L., Platt R.J., Scott D.A., Church G.M., Zhang F. Optical control of mammalian endogenous transcription and epigenetic states. Nature 2013, 500:472-476.
53. Kralj J.M., Douglass A.D., Hochbaum D.R., Maclaurin D., Cohen A.E. Optical recording of action potentials in mammalian neurons using a microbial rhodopsin. Nat. Methods 2012, 9:90-95.
54. Lam A.J., St-Pierre F., Gong Y., Marshall J.D., Cranfill P.J., Baird M.A., McKeown M.R., Wiedenmann J., Davidson M.W., Schnitzer M.J., et al. Improving FRET dynamic range with bright green and red fluorescent proteins. Nat. Methods 2012, 9:1005-1012.
55. Lancaster M.A., Renner M., Martin C.A., Wenzel D., Bicknell L.S., Hurles M.E., Homfray T., Penninger J.M., Jackson A.P., Knoblich J.A. Cerebral organoids model human brain development and microcephaly. Nature 2013, 501:373-379.
56. Lecoq J., Schnitzer M.J. An infrared fluorescent protein for deeper imaging. Nat. Biotechnol. 2011, 29:715-716.
57. Lin J.Y., Lin M.Z., Steinbach P., Tsien R.Y. Characterization of engineered channelrhodopsin variants with improved properties and kinetics. Biophys. J. 2009, 96:1803-1814.
58. Liske H., Towne C., Anikeeva P., Zhao S., Feng G., Deisseroth K., Delp S. Optical inhibition of motor nerve and muscle activity invivo. Muscle Nerve 2013, 47:916-921.
59. Mahou P., Zimmerley M., Loulier K., Matho K.S., Labroille G., Morin X., Supatto W., Livet J., Débarre D., Beaurepaire E. Multicolor two-photon tissue imaging by wavelength mixing. Nat. Methods 2012, 9:815-818.
60. Marshall J.D., Schnitzer M.J. Optical strategies for sensing neuronal voltage using quantum dots and other semiconductor nanocrystals. ACS Nano 2013, 7:4601-4609.
61. Mathieson K., Loudin J., Goetz G., Huie P., Wang L., Kamins T.I., Galambos L., Smith R., Harris J.S., Sher A., Palanker D. Photovoltaic Retinal Prosthesis with High Pixel Density. Nat. Photonics 2012, 6:391-397.
62. Mattis J., Tye K.M., Ferenczi E.A., Ramakrishnan C., O'Shea D.J., Prakash R., Gunaydin L.A., Hyun M., Fenno L.E., Gradinaru V., et al. Principles for applying optogenetic tools derived from direct comparative analysis of microbial opsins. Nat. Methods 2012, 9:159-172.
63. Micheva K.D., Smith S.J. Array tomography: a new tool for imaging the molecular architecture and ultrastructure of neural circuits. Neuron 2007, 55:25-36.
64. Ohkura M., Sasaki T., Sadakari J., Gengyo-Ando K., Kagawa-Nagamura Y., Kobayashi C., Ikegaya Y., Nakai J. Genetically encoded green fluorescent Ca2+ indicators with improved detectability for neuronal Ca2+ signals. PLoS ONE 2012, 7:e51286.
65. Oron D., Tal E., Silberberg Y. Scanningless depth-resolved microscopy. Opt. Express 2005, 13:1468-1476.
66. Owen S.C., Fisher S.A., Tam R.Y., Nimmo C.M., Shoichet M.S. Hyaluronic acid click hydrogels emulate the extracellular matrix. Langmuir 2013, 29:7393-7400.
67. Ozden I., Wang J., Lu Y., May T., Lee J., Goo W., O'Shea D.J., Kalanithi P., Diester I., Diagne M., et al. A coaxial optrode as multifunction write-read probe for optogenetic studies in non-human primates. J.Neurosci. Methods 2013, 219:142-154.
68. Quirin S., Peterka D.S., Yuste R. Instantaneous three-dimensional sensing using spatial light modulator illumination with extended depth of field imaging. Opt. Express 2013, 21:16007-16021.
69. Reynolds B.A., Weiss S. Generation of neurons and astrocytes from isolated cells of the adult mammalian central nervous system. Science 1992, 255:1707-1710.
70. Samara C., Rohde C.B., Gilleland C.L., Norton S., Haggarty S.J., Yanik M.F. Large-scale invivo femtosecond laser neurosurgery screen reveals small-molecule enhancer of regeneration. Proc. Natl. Acad. Sci. USA 2010, 107:18342-18347.
71. Schrödel T., Prevedel R., Aumayr K., Zimmer M., Vaziri A. Brain-wide 3D imaging of neuronal activity in Caenorhabditis elegans with sculpted light. Nat. Methods 2013, 10:1013-1020.
72. Schultheis C., Liewald J.F., Bamberg E., Nagel G., Gottschalk A. Optogenetic long-term manipulation of behavior and animal development. PLoS ONE 2011, 6:e18766.
73. Shenoy K.V., Sahani M., Churchland M.M. Cortical control of arm movements: a dynamical systems perspective. Annu. Rev. Neurosci. 2013, 36:337-359.
74. Sinha S., Liang L., Ho E.T.W., Urbanek K.E., Luo L., Baer T.M., Schnitzer M.J. High-speed laser microsurgery of alert fruit flies for fluorescence imaging of neural activity. Proc. Natl. Acad. Sci. USA 2013, in press.
75. Tam R.Y., Fuehrmann T., Mitrousis N., Shoichet M.S. Regenerative Therapies for Central Nervous System Diseases: a Biomaterials Approach. Neuropsychopharmacology 2013, in press. Published online September 4, 2013.
76. Tanaka K.F., Matsui K., Sasaki T., Sano H., Sugio S., Fan K., Hen R., Nakai J., Yanagawa Y., Hasuwa H., et al. Expanding the repertoire of optogenetically targeted cells with an enhanced gene expression system. Cell Rep 2012, 2:397-406.
77. Testa I., Urban N.T., Jakobs S., Eggeling C., Willig K.I., Hell S.W. Nanoscopy of living brain slices with low light levels. Neuron 2012, 75:992-1000.
78. Tibbitt M.W., Anseth K.S. Dynamic microenvironments: the fourth dimension. Sci. Transl. Med. 2012, 4:60ps24.
79. Urban N.T., Willig K.I., Hell S.W., Nägerl U.V. STED nanoscopy of actin dynamics in synapses deep inside living brain slices. Biophys. J. 2011, 101:1277-1284.
80. Viventi J., Kim D.H., Vigeland L., Frechette E.S., Blanco J.A., Kim Y.S., Avrin A.E., Tiruvadi V.R., Hwang S.W., Vanleer A.C., et al. Flexible, foldable, actively multiplexed, high-density electrode array for mapping brain activity invivo. Nat. Neurosci. 2011, 14:1599-1605.
81. Wang H., Sugiyama Y., Hikima T., Sugano E., Tomita H., Takahashi T., Ishizuka T., Yawo H. Molecular determinants differentiating photocurrent properties of two channelrhodopsins from chlamydomonas. J.Biol. Chem. 2009, 284:5685-5696.
82. Watson B.O., Nikolenko V., Araya R., Peterka D.S., Woodruff A., Yuste R. Two-photon microscopy with diffractive optical elements and spatial light modulators. Front Neurosci 2010, 4.
83. Wilt B.A., Burns L.D., Wei Ho E.T., Ghosh K.K., Mukamel E.A., Schnitzer M.J. Advances in light microscopy for neuroscience. Annu. Rev. Neurosci. 2009, 32:435-506.
84. Wilt B.A., Fitzgerald J.E., Schnitzer M.J. Photon shot noise limits on optical detection of neuronal spikes and estimation of spike timing. Biophys. J. 2013, 104:51-62.
85. Wu F., Stark E., Im M., Cho I.J., Yoon E.S., Buzsáki G., Wise K.D., Yoon E. An implantable neural probe with monolithically integrated dielectric waveguide and recording electrodes for optogenetics applications. J.Neural Eng. 2013, 10:056012.
86. 2+ indicators and photophysical considerations for optogenetic applications. ACS Chem Neurosci 2013, 4:963-972.
87. Xu K., Zhong G., Zhuang X. Actin, spectrin, and associated proteins form a periodic cytoskeletal structure in axons. Science 2013, 339:452-456.
88. Yizhar O., Fenno L.E., Davidson T.J., Mogri M., Deisseroth K. Optogenetics in neural systems. Neuron 2011, 71:9-34.
89. Yizhar O., Fenno L.E., Prigge M., Schneider F., Davidson T.J., O'Shea D.J., Sohal V.S., Goshen I., Finkelstein J., Paz J.T., et al. Neocortical excitation/inhibition balance in information processing and social dysfunction. Nature 2011, 477:171-178.
90. Zhang F., Vierock J., Yizhar O., Fenno L.E., Tsunoda S., Kianianmomeni A., Prigge M., Berndt A., Cushman J., Polle J., et al. The microbial opsin family of optogenetic tools. Cell 2011, 147:1446-1457.
91. Zhao S., Cunha C., Zhang F., Liu Q., Gloss B., Deisseroth K., Augustine G.J., Feng G. Improved expression of halorhodopsin for light-induced silencing of neuronal activity. Brain Cell Biol. 2008, 36:141-154.
92. 2+ indicators. Science 2011, 333:1888-1891.
93. Ziv Y., Burns L.D., Cocker E.D., Hamel E.O., Ghosh K.K., Kitch L.J., El Gamal A., Schnitzer M.J. Long-term dynamics of CA1 hippocampal place codes. Nat. Neurosci. 2013, 16:264-266.